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An extract from the brown alga Bifurcaria bifurcata induces irreversible arrest of cell proliferation in a non-small-cell bronchopulmonary carcinoma line

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Abstract

In this study, the antiproliferative activity of a crude extract isolated from Bifurcaria bifurcata (Velley) Ross, a common marine brown alga of the Atlantic shores of Europe, was investigated. Its antiproliferative effect on asynchronous cells of a human non-small-cell bronchopulmonary carcinoma line (NSCLC-N6), particularly chemo-resistant, was expected in vitro. Cell growth appeared to be inhibited in the G1 phase of the cell cycle, and kinetic studies in pretreated cells showed that this growth arrest was irreversible. These events are related to a terminal differentiation induction.

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References

  • Barlogie B, Drewinko B, Johnston DA, Buchner T, Hauss WH, Freireich EJ (1976) Pulse cytophotometric analysis of synchronised cells in vitro. Cancer Res. 36:1176–1181.

    PubMed  CAS  Google Scholar 

  • Bergé JP, Bourgougnon N, Carbonelle D, Le Bet V, Tomasoni C, Durand P, Roussakis C (1997) Antiproliferative effects of an organic extract from the marine diatom Skeletonema costatum against a non-small-cell bronchopulmonary carcinoma line (NSCLC-N6). Anticancer Res. 17: 2115–2120.

    PubMed  Google Scholar 

  • Blunt JW, Copp BR, Munro MHG, Northcote PT, Prinsep MR (2003) Marine natural products. Nat. Prod. Rep. 20: 1–48.

    Article  PubMed  CAS  Google Scholar 

  • Boisson-Vidal C, Haroun F, Ellouali M, Blondin C, Jozefonvicz J (1995) Biological activities of polysaccharides from marine algae. Drugs of the future 20: 1237–1249.

    Google Scholar 

  • Bourgougnon N, Roussakis C, Kornprobst JM, Lahaye M (1994) Effects in vitro of sulfated polysaccharide from Schizymenia dubyi (Rhodophyta, Gigartinales) on a non-small-cell bronchopulmonary carcinoma line (NSCLC-N6). Cancer Lett. 85, 87.

    Article  Google Scholar 

  • Cañedo LM, de la Fuente JA, Gesto C, Ferreiro MJ, Jiménez C, Riguera R (1999) Agrochelin, a new cytotoxic alkaloid from the marine bacteria Agrobacterium sp. Tet. Lett. 40: 6841–6844.

    Article  Google Scholar 

  • Carbonelle D, Pondaven P, Morançais M, Massé G, Bosch S, Jacquot C, Briand G, Robert JM, Roussakis C (1999) Antitumor and antiproliferative effects of an aqueous extract from the marine diatom Haslea ostrearia (Simonsen) against solid tumor: lung carcinoma (NSCLC-N6), kidney carcinoma (E39) and melanoma (M96) cell lines. Anticancer Res. 19: 621–624.

    PubMed  Google Scholar 

  • Culioli G, Ortalo–Magne A, Richou M, Valls R, Piovetti L (2002) Seasonal variations in the chemical composition of Bifurcaria bifurcata (Cystoseiraceae). Biochem. Syst. Ecol. 30: 61–64.

    Article  CAS  Google Scholar 

  • Deslandes E, Pondaven P, Auperin T, Roussakis C, Guézennec J, Stiger V, Payri C (2000) Preliminary study of the in vitro antiproliferative effect of a hydroethanolic extract from the subtropical seaweed Turbinaria ornata (Turner) J. Agardh on a human non small cell bronchopulmonary carcinoma line (NSCLC-N6). J. Appl. Phycol. 12: 257–262.

    Article  Google Scholar 

  • Duran R, Zubia E, Ortega MJ, Salva J (1997) New diterpenoids from the alga Dictyota dichotoma. Tetrahedron 53: 8675–8688.

    Article  CAS  Google Scholar 

  • Faulkner DJ (2000) Marine pharmacology. Int. J. Gen. Mol. Micr. 77: 135–145.

    CAS  Google Scholar 

  • Fried J, Mandel M (1979) Multi-user system for analysis of data from flow cytometry. Comp. Prog. Biomed. 10: 218–230.

    Article  CAS  Google Scholar 

  • Fuller RW, Cardellina II JH, Jurek J, Scheuer PJ, Alvarado-Linder B, McGuire M, Gray GN, Steiner JR, Clardy J, Menez E, Newman DJ, Snader KM, Boyd MR (1994) Isolation and structure/activity features of halomon-related antitumor monoterpenes from the red alga Portieria hornemannii. J. Med. Chem. 37: 4407–4411.

    Article  PubMed  CAS  Google Scholar 

  • Hamann MT, Otto CS, Scheuer PJ, Dunbar DC (1996) Kahalalides: Bioactive peptides from a marine mollusk Elysia rufescens and its algal diet Bryopsis sp. J. Org. Chem. 61: 6594–6600.

    Article  PubMed  CAS  Google Scholar 

  • Harada H, Kamei Y (1998) Dose-dependent selective cytotoxicity of extracts from marine green alga, Cladophoropsis vaucheriaeformis, against mouse leukemia L1210 cells. Biol. Pharm. Bull. 21: 386–389.

    PubMed  CAS  Google Scholar 

  • Harada H, Noro T, Kamei Y (1997) Selective antitumor activity in vitro from marine algae from Japan coasts. Biol. Pharm. Bull. 20: 541–546.

    PubMed  CAS  Google Scholar 

  • Harris H (1990) The role of the differentiation in the suppression of malignacy. J. Cell Sci. 97: 5–10.

    PubMed  Google Scholar 

  • Hellio C, Thomas-Guyon H, Culioli G, Piovetti L, Bourgougnon N, Le Gal Y (2001) Marine Antifoulants from Bifurcaria bifurcata (Phaeophyceae, Cystoseiraceae) and other Brown Macroalgae. Biofouling 17: 189–201.

    CAS  Google Scholar 

  • Ihde DC, Pass HL, Llastein EJ (1993) Small cell lung cancer, in: V.T. De Vita, S. Hellman, S.A. Rosenberg (ed.) Cancer Principles and Practice of Oncology, Lippincott: Philadelphia, pp. 673–723.

  • Ishitsuka MO, Kusumi T, Ichikawa A, Kakisawa H (1990) Bicyclic diterpenes from two species of brown algae of the Dictyotaceae. Phytochem. 29: 2605–2610.

    Article  CAS  Google Scholar 

  • Lotan R, Francis GE, Freeman CS, Vaxman S (1990) Differentiation therapy. Cancer Res. 50: 3453–3464.

    PubMed  CAS  Google Scholar 

  • Mason MD (1992) Differentiation and cancer. Eur. J. Cancer 28: 255–258.

    Article  PubMed  CAS  Google Scholar 

  • Maurer HR, Eckert K, Bissery MC (1993) Taxotere inhibits the proliferation and induces the differentiation of HL-60 and K562 human myeloid leukemia cell in vitro. Int. J. Oncol. 3: 161–165.

    CAS  Google Scholar 

  • Mayer AM, Gustafson KR (2003) Marine pharmacology in 2000: Antitumor and cytotoxic compounds. Int. J. Cancer 105: 291–299.

    Article  PubMed  CAS  Google Scholar 

  • Minna D, Higgins GA, Galstein EL (1982) Cancer of the lung, in: V.T. De Vita, S. Hellman and S.A. Rosenberg (ed.) Cancer Principles and Practice of Oncology, Lippincott: Philadelphia, pp. 389–398.

  • Morimoto T, Nagatsu A, Murakami N, Sakakibara J, Tokuda H, Nishino H, Iwashima A (1995) Anti-tumour-promoting glyceroglycolipids from the green alga, Chlorella vulgaris. Phytochem. 40: 1433–1437.

    Article  CAS  Google Scholar 

  • Mossmann T (1983) Rapid colorimetric assay cellular growth and survival: Application to proliferation and cytotoxicity assay. J. Immunol. Methods 65: 55–63.

    Article  PubMed  Google Scholar 

  • Numata A, Kanbara S, Takahashi C, Fujiki R, Yoneda M, Fujita E, Nabeshima Y (1991) Cytotoxic activity of marine algae and a cytotoxic principle of the brown alga Sargassum tortile. Chem. Pharm. Bull. 39: 2129–2131.

    PubMed  CAS  Google Scholar 

  • O'Farell PH, Edgrad BA, Lakich D, Lehner CF (1989). Directing cell division during development. Science 246: 635–640.

    Article  PubMed  Google Scholar 

  • Okai Y, Higashi-Okai K, Nakamura S, Yano Y, Otani S (1994) Suppressive effects of the extracts of Japanese edible seaweeds on mutagen-induced umu C gene expression in Salmonella typhimurium (TA 1535/pSK 1002) and tumor promotor-dependent ornithine decarboxylase induction in BALB/c 3T3 fibroblast cells. Cancer Lett. 87: 25–32.

    Article  PubMed  CAS  Google Scholar 

  • Pec MK, Moser-Thier K, Fernadez JJ, Souto ML, Kubista E (1999) Growth inhibition by dehydrothyrsiferol—a non-Pgp modulator, derived from a marine red alga—in human breast cancer cell lines. Int. J. Oncol. 14: 739–743.

    PubMed  CAS  Google Scholar 

  • Ortalo-Magné A, Culioli G, Valls R, Pucci B, Piovetti L (2005) Polar acyclic diterpenoids from Bifurcaria bifurcata (Fucales, Phaeophyta). Phytochem. 66: 2316–2323.

    Article  CAS  Google Scholar 

  • Riou D, Roussakis C, Robillard N, Biard JF, Verbist JF (1993) Bistramide A-induced irreversible arrest of cell proliferation in a non small-cell bronchopulmonary carcinoma is similar to induction of terminal maturation Bio. Cell 77: 261–264.

    CAS  Google Scholar 

  • Riou D, Colliec-Jouault S, Pinczon Du Sel S, Bosch S, Siavoshian S, Le Bert V, Tomasoni C, Sinsuin C, Durand P, Roussakis C (1996) Antitumor and antiproliferative effects of a fucan extracted from Ascophyllum nodosum against a non-small-cell bronchopulmonary carcinoma line. Anticancer Res. 16: 1213–1218.

    PubMed  CAS  Google Scholar 

  • Roussakis C, Gratas C, Audoin AF, Le Boterf J, Dabouis G, Verbist JF (1991) Study of in vitro drug sensitivity on a newly established cell line from a primary bronchial epidermoid carcinoma of human origin (NSCLC-N6). Anticancer Res. 11: 2239–2244.

    PubMed  CAS  Google Scholar 

  • Salvati F, Teodori L, Gagliardi L, Signora M, Aquilini M, Storniello G (1989) DNA flow cytometric studies of 66 human lung tumors analyzed before treatment. Chest. 96, 1092–1098.

    Article  PubMed  CAS  Google Scholar 

  • Siavoshian S, Bosch S, Pondaven P, Moré MT, Riou D, Dabouis G, André MJ, Roussakis C (1998). Cloning of human cancer cell line (NSCLC–N6) and comparative study of the clones in vitro. Anticancer Res. 18: 193–200.

    PubMed  CAS  Google Scholar 

  • Trimurtulu G, Ohtani I, Patterson GML, Moore RE, Corbett TH, Valeriote FA, Demchik (1994) Total structures of cryptophycins, potent antitumor depsipeptides from the blue-green alga Nostoc sp. strain GSV 224. J. Am. Chem. Soc. 116: 4729–4737.

    Article  CAS  Google Scholar 

  • Urones JG, Basabe P, Marcos IS, Pineda J, Lithgow AM, Moro RF, Brito Palma FMS, Araujo MEM, Gravalos DG (1992a) Meroterpenes from Cystoseira usneoides Phytochem. 31: 179–182.

    Article  CAS  Google Scholar 

  • Urones JG, Araujo MEM, Brito Palma FMS, Basabe P, Marcos IS, Moro, RF, Lithgow AM, Pineda J (1992b) Meroterpenes from Cystoseira usneoides II. Phytochem. 31: 2105–2109.

    Article  CAS  Google Scholar 

  • Valls R, Banaigs B, Francisco C, Codomier L, Cave A (1986) An acyclic diterpene from the brown alga Bifurcaria bifurcata. Phytochem. 25: 751–752.

    Article  CAS  Google Scholar 

  • Valls R, Banaigs B, Piovetti L, Zerzouf A (1993) Variations géographiques de la composition en diterpènes de Bifurcaria bifurcata des côtes atlantiques marocaines. Ann. Inst. Ocean. 63: 215–223.

    Google Scholar 

  • Vindelov LL (1977) Flow microfluorimetric analysis of nuclear DNA in cells from solid tumors and cells suspensions. A new method for rapid isolation and staining of nuclei. Virshows Arch. B. Cell Pathol. 24: 227–242.

    CAS  Google Scholar 

  • Wille JJ, Scott RE (1982) Topography of the predifferentiation GD growth arrest state relative to other growth arrest states in the G1-phase of the cell cycle. Int. J. Cell Physiol. 112: 115–122.

    Article  CAS  Google Scholar 

  • Wille JJ, Scott RE (1986) Suppression of tumoregenicity by the cell cycle dependent control of cellular differentiation and proliferation. Int. J. Cancer. 37: 875–881.

    Article  PubMed  Google Scholar 

  • Williams CJ (1989) Chemotherapy of non-small-cell lung cancer carcinoma line (NSCLC-N6). Br. J. Cancer. 60, 9–12.

    PubMed  CAS  Google Scholar 

  • Zee OP, Kim DK, Choi SU, Lee CO, Lee KR, (1999) A new cytotoxic acyclic diterpene from Carpesium divaricatum. Arch. Pharm. Res. 22: 225–227.

    Article  PubMed  CAS  Google Scholar 

  • Ziddane M, Pondaven P, Roussakis C, More MT (1996) Effects in vitro of Pachymatismin, a glycoprotein from the marine sponge Pachymatisma johnstonii, on a non-small-cell bronchopulmonary carcinoma line. Anticancer Res. 16: 2800–2812.

    Google Scholar 

  • Zimmermann PV, Hawson GAT, Bint HH, Parsons PG (1987) Ploidy as a pronostic determinant in surgically treated lung cancer. Lancet. 2: 530–533.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. ISOMer, Faculté de Pharmacie, 1 Rue Gaston Veil, F44035, Nantes, France

    Dimitri Moreau, Catherine Jacquot, Marcel Jugé & Christos Roussakis

  2. Laboratoire de Biologie et d'Environnement Marin, Avenue Crépeau, Université de La Rochelle, F17042, La Rochelle cedex 01, France

    Hélène Thomas-Guyon

  3. Laboratoire des Matériaux à Finalités Spécifiques, équipe “Chimie des Produits Naturels Marins,” Avenue de l'Université, Université du Sud Toulon-Var, BP 20132, F83957, La Garde cedex, France

    Gérald Culioli, Annick Ortalo-Magné & Louis Piovetti

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  1. Dimitri Moreau
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  2. Hélène Thomas-Guyon
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  3. Catherine Jacquot
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Correspondence to Dimitri Moreau.

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Moreau, D., Thomas-Guyon, H., Jacquot, C. et al. An extract from the brown alga Bifurcaria bifurcata induces irreversible arrest of cell proliferation in a non-small-cell bronchopulmonary carcinoma line. J Appl Phycol 18, 87–93 (2006). https://doi.org/10.1007/s10811-005-9019-1

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